A global molecular phylogeny yields insights into the dispersal and invasion history of Junonia, a butterfly genus with remarkable dispersal abilities

Abstract

The nymphalid butterfly genus Junonia has remarkable dispersal abilities. Occurring on every continent except Europe and Antarctica, Junonia are often among the only butterflies on remote oceanic islands. The biogeography of Junonia has been controversial, plagued by taxonomic disputes, small phylogenetic datasets, incomplete taxon sampling, and shared interspecific mitochondrial haplotypes. Junonia originated in Africa but its route into the New World remains unknown. Presented here is, to our knowledge, the most comprehensive Junonia phylogeny to date, using full mitogenomes and nuclear ribosomal RNA repeats from 40 of 47 described species. Junonia is monophyletic and the genus Salamis is its probable sister clade. Genetic exchange between Indo-Pacific Junonia villida and New World Junonia vestina is evident, suggesting a trans-Pacific route into the New World. However, in both phylogenies, the sister clades to most New World Junonia contain both African and Asian species. Multiple trans-Atlantic or trans-Pacificinvasions could have contributed to New World diversification. Hybridization and lateral transfer of mitogenomes, already well-documented in New World Junonia, also occurs in at least two Old World lineages (Junonia orithya/Junonia hierta and Junonia iphita/Junonia hedonia). Variation associated with reticulate evolution creates challenges for phylogenetic reconstruction, but also may have contributed to patterns of speciation and diversification in this genus.

Keywords: Junonia; Junoniini; evolutionary radiation; mitogenomics; phylogenomics; reticulate evolution.

Figure 1.

Hypotheses for the phylogeny of Junonia with proposed sister groups to the New World Junonia: (a) Junonia villida by Forbes [14,15], (b) African Junonia orithya madagascariensis by Eliot [12,13] and (c) Asian Junonia orithya orithya by Corbet [11] based on morphology; (d) presents the molecular phylogeny of Kodandaramaiah & Wahlberg [3] and Kodandaramaiah [9] as interpreted by McCullagh [10].

Figure 2.

Junonia mitogenome Bayesian inference phylogeny (GTR + I + G model, best state likelihood = −170 867 and a deviation of split frequencies = 0.002109). Sixty-four Junonia mitogenomes, 21 other tribe Junoniini mitogenomes and 12 mitogenomes from other Nymphalinae tribes. The MrBayes Bayesian posterior probability values are given at each node. (Online version in colour.)

Figure 3.

Junonia complete rRNA repeat Bayesian inference phylogeny (GTR + I + G model, best state likelihood = −119 000 and an average deviation of split frequencies = 0.003566) based on 62 Junonia specimens, 19 other sequences from tribe Junoniini and nine outgroup species from tribes within subfamily Nymphalinae. The Bayesian posterior probability values determined by MrBayes are given at each node. (Online version in colour.)

Figure 4.

Modified molecular phylogeny of the Old World Junonia. Interpretations based on mitogenome and rRNA repeat phylogenetic reconstructions from figures 2 and 3. Geographical origins, habitat preferences and the display of mimicry of lineages are indicated. (Online version in colour.)